1.Eye size varies notably across taxa. Much work suggests that this variation is driven by contrasting ecological selective pressures. However, evaluations of the relationship between ecological factors and shifts in eye size have largely occurred at the macroevolutionary scale. Experimental tests in nature are conspicuously absent. 2.Trinidadian killifish, Rivulus hartii, are found across fish communities that differ in predation intensity. We recently showed that increased predation is associated with the evolution of a smaller eye. Here, we test how divergent predatory regimes alter the trajectory of eye size evolution using comparative mark‐recapture experiments in multiple streams. 3.We found that increases in eye size are associated with enhanced survival, irrespective of predation intensity. More importantly, eye size is associated with enhanced growth in communities that lack predators, while this trend is absent when predators are present. 4.Such results argue that increased competition for food in sites that lack predators is the key driver of eye size evolution.